The variety in the Burgess Shale was so extreme it took several decades for paleontologists to grasp it fully. Walcott, for instance, attempted to fit all of the new forms into existing phyla. However, even in the midst of this attempt, he realized that this revolutionary quarry posed a problem more fundamental than a need to tidy up the existing taxonomy. He had met Louis Agassiz at a young age, having sold him some of his first fossils, and later described him as “a guide in whom I could trust and follow,” one in whose work “I find this tribute to the Great Mind that created the objects of his study.”10 But in the great debate between Agassiz and Darwin, Walcott sided with the Englishman. Thus, the Burgess Shale struck Walcott as not only fascinating, but puzzling.
A Puzzling Pattern
Over the years, as paleontologists have reflected on the overall pattern of the Precambrian–Cambrian fossil record in light of Walcott’s discoveries, they too have noted several features of the Cambrian explosion that are unexpected from a Darwinian point of view11 in particular: (1) the sudden appearance of Cambrian animal forms; (2) an absence of transitional intermediate fossils connecting the Cambrian animals to simpler Precambrian forms; (3) a startling array of completely novel animal forms with novel body plans; and (4) a pattern in which radical differences in form in the fossil record arise before more minor, small-scale diversification and variations. This pattern turns on its head the Darwinian expectation of small incremental change only gradually resulting in larger and larger differences in form.
The Missing Tree
Figures 2.7 and 2.8 illustrate the difficulty posed by the first two of these features: sudden appearance and missing intermediates. These diagrams graph morphological change over time. The first shows the Darwinian expectation that changes in morphology should arise only as tiny changes accumulate. This Darwinian commitment to gradual change through microevolutionary variations produces the classic representation of evolutionary history as a branching tree.
Now compare this branching tree pattern with the pattern in the fossil record. The bottom part of Figure 2.7 and Figure 2.8 show that the Precambrian strata do not document the expected transitional intermediates between Cambrian and Precambrian fauna. Instead, the Precambrian–Cambrian fossil record, especially in light of the Burgess Shale after Walcott, points to the geologically sudden appearance of complex and novel body plans.
FIGURE 2.7
The origin of animals. Darwinian theory (top) predicts gradual evolutionary change in contrast to the fossil evidence (bottom), which shows the abrupt appearance of the major animal groups.
FIGURE 2.8
According to Darwinian theory, the strata beneath the Cambrian rocks should evidence many ancestral and intermediate forms. Such forms have not been found for the vast majority of animal phyla. These anticipated but missing forms are represented by the gray circles. Lines and dark circles depict fossilized representatives of phyla that have been found.
Of course, the fossil record does show an overall increase in the complexity of organisms from Precambrian to Cambrian times, as Darwin expected. But the problem posed by the Burgess Shale is not the increase in complexity, but the sudden quantum leap in complexity. The jump from the simpler Precambrian organisms (further explored in the next chapters) to the radically different Cambrian forms appears to occur far too suddenly to be readily explained by the gradual activity of natural selection and random variations. Neither the Burgess Shale nor any other series of sedimentary strata known in Walcott’s day recorded a pattern of novel body plans arising gradually from a sequence of intermediates. Instead, completely unique organisms such as the bizarre arthropod Opabinia (see Fig. 2.9)—with its fifteen articulated body segments, twenty-eight gills, thirty flipper-like swimming lobes, long trunk-like proboscis, intricate nervous system, and five separate eyes12—appear fully formed in the Cambrian strata along with representatives of other fundamentally different body plans and designs of equal complexity.
Darwin, as we know, regarded the sudden appearance of the Cambrian animals as a significant challenge to his theory.13 Where natural selection had to bridge yawning chasms from relatively simple life-forms to exquisitely complex creatures, it would require great expanses of time.14
FIGURE 2.9
Figure 2.9a (top): Artist rendering of Opabinia. Figure 2.9b (bottom): Photograph of Opabinia fossil.
Darwin’s recognition15 of this constraint was prescient. Geologists in his day employed relative dating methods. They did not have modern radiometric methods for determining the “absolute” ages of rocks. For this reason, they did not yet fully understand how long it would have taken to accumulate the great columns of sedimentary rock and, thus, the great expanses of time that were available to the evolutionary process. Neither had scientists yet discovered the sophisticated inner workings of the cell, and the information-rich structures (DNA, RNA, and proteins) that had to be significantly altered to achieve even modest evolutionary changes. Nevertheless, Darwin was able—based upon what he knew of the complexity of organisms and his own understanding of how the mechanism of natural selection must operate—to deduce that descent with modification required time, and lots of it.
Recalling the context of Darwin’s original argument reveals why. In the Origin, he sought to counter the famous watch-to-watchmaker design argument offered by theologian William Paley. Paley had argued that just as complex structures such as watches necessarily issue from intelligent watchmakers, the complex structures in living organisms must likewise owe their origin to a designing intelligence. With natural selection, Darwin proposed a purely natural mechanism for constructing the complex organs and structures (such as eyes) present in many forms of life. His mechanism of natural selection worked by constructing such systems one tiny step at a time, discarding the harmful variations and seizing upon the rare improvement. If evolution progressed by “whole watches”—that is, by entire anatomical systems like the trilobite’s eye—then biology would have fallen back to the old absurdity of imagining that a watch could fall together purely at random and all at once. Thus, unless Darwin’s evolutionary mechanism worked gradually by preserving the tiniest of random changes over many millions of years, it didn’t work at all.
More Missing Links
Two other features of the Cambrian explosion revealed in the Burgess Shale, features (3) and (4) described earlier, not only confirmed the reality of the Cambrian mystery, but broadened and deepened it—and at just the time when paleontologists were looking to resolve the mystery with new fossil discoveries.
First, the great profusion of completely novel forms of life in the Burgess assemblage (feature 3) demanded even more transitional forms than had previously been thought missing. Each new and exotic Cambrian creature—the anomalocarids (see Fig. 2.10), Marrella, Opabinia, and the bizarre and appropriately named Hallucigenia—for which there were again no obvious ancestral forms in the lower strata, required its own series of transitional ancestors. But where were they?
FIGURE 2.10
Figure 2.10a (top): Artist rendering of Anomalocaris. Figure 2.10b (bottom): Photograph of Anomalocaris fossil. Courtesy J. Y. Chen.
Darwin had hoped that later fossil discoveries would eventually eliminate what he regarded as the one outstanding anomaly associated with his theory. Walcott’s discovery was not that discovery. Not only did the Burgess Shale fail to reveal the expected ancestral precursors of the known Cambrian animal forms, but it revealed a motley crew of previously unknown animal forms and body plans that now demanded their own lengthy chain of evolutionary precursors, only complicating the task of explaining the Cambrian explosion in Darwinian terms.
Orders from the Top
The Burgess Shale raised an additional difficulty (feature 4, discussed earlier), though not one that Walcott recognized during his lifetime. Instead, its exposition would await a later generation of Cambrian experts, particularly Stephen Jay Gould. Darwin’s theory implied that as new animal forms first began to emerge from a common
ancestor, they would at first be quite similar to each other, and that large differences in the forms of life—what paleontologists call disparity—would only emerge much later as the result of the accumulation of many incremental changes. In its technical sense, disparity refers to the major differences in form that separate the higher-level taxonomic categories such as phyla, classes, and orders. In contrast, the term diversity refers to minor differences among organisms classified as different genera or species. Put another way, disparity refers to life’s basic themes; diversity refers to the variations on those themes. The more body plans in a fossil assembly, the greater the disparity. And the animal forms preserved in the Burgess Shale display considerable disparity. Further, the large differences in form between the first animals appeared suddenly in the Burgess Shale, and the appearance of such disparity arose before, not after, the diversification of many representatives of lower taxonomic categories (such as species or genera) within each higher category, designating a new body plan.
The site of the Burgess Shale and its setting nicely illustrates the difference between diversity and disparity. Walcott’s celebrated quarry is tucked away in the Canadian Rockies near the Continental Divide. Reaching it involves a six-mile hike through the picturesque scenery of Yoho National Park—Takakkaw Falls, Emerald Lake, and glaciers and glacier-cut mountain peaks thrusting into view at almost every turn. In this ecologically diverse setting, hikers have a chance of spotting squirrels, marmots, deer, moose, elk, wolves, and mountain goats. Rare sightings might include a grizzly bear or Canadian lynx, while alert birdwatchers might glimpse a horned lark, a white-tailed ptarmigan, the rare water pipit, or a gray-crowned rosy finch; an eagle, hawk, or grassland falcon; dippers, jays, migrating warblers, or harlequin ducks.16
As richly various as this array of animals is, all of them come from a single phylum, Chordata—and even from a single subphylum, Vertebrata. Imagine hiking to the quarry to excavate it and, on the hike, being lucky enough to spot every one of these animals along the way. After having feasted your eyes on such animal variety, when you arrive at Walcott’s quarry, it yields not merely dozens of fossilized species from a single subphylum, but wildly disparate creatures from dozens of phyla.
According to Darwin’s theory, the differences in form, or “morphological distance,” between evolving organisms should increase gradually over time as small-scale variations accumulate by natural selection to produce increasingly complex forms and structures (including, eventually, new body plans). In other words, one would expect small-scale differences or diversity among species to precede large-scale morphological disparity among phyla. As the former Oxford University neo-Darwinian biologist Richard Dawkins puts it, “What had been distinct species within one genus become, in the fullness of time, distinct genera within one family. Later, families will be found to have diverged to the point where taxonomists (specialists in classification) prefer to call them orders, then classes, then phyla.”17
Darwin himself made this point in On the Origin of Species. Explaining his famous tree diagram (see Fig. 2.11a), he noted that it illustrated more than just the theory of universal common descent. The tree diagram also illustrated how higher taxa should emerge from lower taxa by the accumulation of numerous slight variations. He said, “The diagram illustrates the steps by which small differences distinguishing varieties are increased into larger differences distinguishing species.”18 He went on to assert that the process of modification by natural selection would eventually move beyond the formation of species and genera to form “two distinct families, or orders, according to the amount of divergent modification supposed to be represented in the diagram.”19 In his view, this process would continue until it produced differences in form that were great enough that taxonomists would classify them as new classes or phyla. In short, diversity would precede disparity, and phyla-level differences in body plan would emerge only after species-, genus-, family-, order-, and class-level differences appeared.
The actual pattern in the fossil record, however, contradicts this expectation (compare Fig. 2.12 to Fig. 2.11b). Instead of more and more species eventually leading to more genera, leading to more families, orders, classes, and phyla, the fossil record shows representatives of separate phyla appearing first followed by lower-level diversification on those basic themes.
This is nowhere more dramatically apparent than in the Cambrian period explains Roger Lewin in the journal Science: “Several possible patterns exist for the establishment of higher taxa, the two most obvious of which are the bottom-up and the top-down approaches. In the first, evolutionary novelties emerge, bit by bit. The Cambrian explosion appears to conform to the second pattern, the top-down effect.”20 Or as paleontologists Douglas Erwin, James Valentine, and Jack Sepkoski note in their study of skeletonized marine invertebrates: “The fossil record suggests that the major pulse of diversification of phyla occurs before that of classes, classes before that of orders, orders before that of families… . The higher taxa do not seem to have diverged through an accumulation of lower taxa.”21 In other words, instead of a proliferation of species and other representatives of lower-level taxa occurring first and then building to the disparity of higher taxa, the highest taxonomic differences such as those between phyla and classes appear first (instantiated by relatively few species-level representatives). Only later, in more recent strata, does the fossil record document a proliferation of representatives of lower taxa: different orders, families, genera, and so on. Yet we would not expect the neo-Darwinian mechanism of natural selection acting on random genetic mutations to produce the top-down pattern that we observe in the history of life following the Cambrian explosion.
FIGURE 2.11
Figure 2.11a (top): Darwin’s theory of common descent illustrated here with his famous branching tree of life diagram reproduced from the Origin of Species, 1859. Figure 2.11b (bottom): Growth of the tree of life over time in the manner envisioned by Darwin with new species giving rise to new genera and families, eventually giving rise to new orders, classes, and phyla (these higher taxonomic categories not depicted).
Of course, advocates of modern phylogenetic classification, with their “rank-free” approach, don’t describe this phenomenon as a “top-down” pattern, because their system of classification dispenses with taxonomic ranks and hierarchies. In their system, there is no “top” and no “down.” Nevertheless, advocates of phylogenetic classification do acknowledge that different combinations of “character” states (characteristics or features of organisms) can mark either bigger or smaller morphological differences between clades (closely related groups of organisms that presumably share a common ancestor). And some leading advocates of phylogenetic classification have noted that the fossil record exhibits a pattern in which a few character traits marking large morphological differences between clades arise first, followed later in each clade by the addition of other combinations of characters that mark smaller differences within those clades. Larger differences between clades arise first, smaller differences within them arose later—the themes precede the variations.
FIGURE 2.12
The top-down pattern of appearance in the fossil record: disparity precedes diversity.
The founder of the modern phylogenetic classification, Willi Hennig, for example, noted that once particular groups arise, the range of allowable variability within those groups narrows. In his classic work Phylogenetic Systematics, Hennig quoted another paleontologist approvingly who observed: “The breadth of evolution of successive groups shows a distinct narrowing, since the basic divergences of organization became progressively smaller. The type of mammals is more uniform and closed than that of the reptiles, which in turn is unquestionably uniform compared to that of the Amphibia-Stegocephalia.” Hennig goes on to explain that “the same phenomenon is repeated in every systematic unit of higher or lower order.”22
Yet, on a Darwinian view, small-scale variations and differences should arise first, gradually giving rise to lar
ger-scale differences in form—just the opposite of the pattern evident in the fossil record. Thus, the discovery, and later analysis, of the Burgess revealed another puzzling feature of the fossil record from a Darwinian point of view, regardless of which system of classification paleontologists prefer to use. Indeed, Walcott’s discovery turned Darwin’s anticipated bottom-up—or small changes first, big changes later—pattern on its head.
First Impressions
The extraordinary conditions at work in the preservation of the Burgess fauna helped to reveal the extent of the rich diversity (and disparity) of form present in the Cambrian period. On shale of a very fine grain, the Burgess fossils look like lithographic pictures, dark on light (see color insert plates 15 and 16). Even the soft parts like the gills and guts are sometimes preserved. This is not the norm in the world of paleontology. Usually soft tissues decay before they can be fossilized, leaving behind only harder parts, such as bone, teeth, and shells, to be preserved. The Burgess event that captured the Cambrian fauna for future discovery was different. Although it took the lives of untold Cambrian animals, it did so with an exquisite delicacy that preserved soft tissue.
Visualizing how this occurred will drive home why the conditions were so unusual. All of the fossilized animals of the Burgess Shale were sea creatures living near an enormous carbonate reef that later was thrust upward by plate tectonic activity to form what is now called the Cathedral Escarpment. Long after the sea creatures of the Burgess Shale were entombed, these tectonic forces drove the fossils upward from the seafloor carrying them many miles eastward along faults, at the same time building the mountains that Walcott would climb millions of years later.
Thanks to this tectonic movement of earth’s major plates, the continents are now located in very different places than they were millions of years ago. At the time these Cambrian creatures were alive, the land masses that would later form North America lay on the equator.
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